Capturing one of the human gut microbiome's most wanted: Reconstructing the genome of a novel butyrate-producing, clostridial scavenger from metagenomic sequence data

Frontiers in Microbiology

Volumn 7, Issue MAY, 2016, Pages

  Jeraldo, Patricio ^a,b   Hernandez, Alvaro ^b   Nielsen, Henrik B ^c   Chen, Xianfeng ^a   White, Bryan A ^b   Goldenfeld, Nigel ^b,d   Nelson, Heidi ^a   Alhquist, David ^a   Boardman, Lisa ^a   Chia, Nicholas ^a,e  

^a MAYO CLINIC   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^d University of Illinois at Urbana Champaign   (United States)

^e MAYO GRADUATE SCHOOL   (United States)

Author keywords

Binning; Butyricicoccus; Genome assembly; Metagenomics; Microbiome

Indexed keywords

ARTICLE; CASE REPORT; COLON CANCER; DNA DNA HYBRIDIZATION; DNA SEQUENCE; GENE MAPPING; HUMAN; INFLAMMATORY BOWEL DISEASE; INTESTINE FLORA; METAGENOMICS; MICROBIAL IDENTIFICATION; MICROBIAL METABOLISM; MICROBIOME; PHYLOGENY; POLYMERASE CHAIN REACTION; RNA PROCESSING;

EID: 84973482180     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.00783     Document Type: Article

References (67)

1. Albertsen, M., Hugenholtz, P., Skarshewski, A., Nielsen, K. L., Tyson, G. W., and Nielsen, P. H. (2013). Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes. Nat. Biotechnol. 31, 533-538. doi: 10.1038/nbt.2579
2. Al-Hinai, M., Jones, S., and Papoutsakis, E. (2015). The Clostridium sporulation programs: diversity and preservation of endospore differentiation. Microbiol. Mol. Biol. Rev. 79, 19-37. doi: 10.1128/MMBR.00025-14
3. Alneberg, J., Bjarnason, B. S., de Bruijn, I., Schirmer, M., Quick, J., Ijaz, U. Z., et al. (2013). CONCOCT: Clustering cONtigs on COverage and ComposiTion. arXiv: 1312.4038
4. Altschul, S., Gish, W., Miller, W., Myers, E., and Lipman, D. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403-410. doi: 10.1016/S0022-2836(05)80360-2
5. Bankevich, A., Nurk, S., Antipov, D., Gurevich, A. A., Dvorkin, M., Kulikov, A. S., et al. (2012). SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455-477. doi: 10.1089/cmb.2012.0021
6. Bodenhofer, U., Kothmeier, A., and Hochreiter, S. (2011). APCluster: an R package for affinity propagation clustering. Bioinformatics 27, 2463-2464. doi: 10.1093/bioinformatics/btr406
7. Boisvert, S., Raymond, F., Godzaridis, E., Laviolette, F., and Corbeil, J. (2012). Ray Meta: scalable de novo metagenome assembly and profiling. Genome Biol. 13:R122. doi: 10.1186/gb-2012-13-12-r122
8. Bokkenheuser, V., Winter, J., Morris, G., and Locascio, S. (1986). Steroid desmolase synthesis by Eubacterium desmolans and Clostridium cadavaris. Appl. Environ. Microbiol. 52, 1153-1156
9. Bolger, A. M., Lohse, M., and Usadel, B. (2014). Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114-2120. doi: 10.1093/bioinformatics/btu170
10. Brettin, T., Davis, J. J., Disz, T., Edwards, R. A., Gerdes, S., Olsen, G. J., et al. (2015). RASTtk: a modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Sci. Rep. 5:8365. doi: 10.1038/srep08365
11. Caporaso, J., Bittinger, K., Bushman, F., DeSantis, T., Andersen, G., and Knight, R. (2010). PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26, 266-267. doi: 10.1093/bioinformatics/btp636
12. Chen, J., Ryu, E., Hathcock, M., Ballman, K., Chia, N., Olson, J. E., et al. (2016). Impact of demographics on human gut microbial diversity in a US Midwest population. PeerJ 4:e1514. doi: 10.7717/peerj.1514
13. Chu, J., Sadeghi, S., Raymond, A., Jackman, S., Nip, K., Mar, R., et al. (2014). BioBloom tools: fast, accurate and memory-efficient host species sequence screening using bloom filters. Bioinformatics 30, 3402-3404. doi: 10.1093/bioinformatics/btu558
14. Cole, J. R., Wang, Q., Cardenas, E., Fish, J., Chai, B., Farris, R. J., et al. (2009). The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 37, D141-D145. doi: 10.1093/nar/gkn879
15. Crusoe, M. R., Alameldin, H. F., Awad, S., Boucher, E., Caldwell, A., Cartwright, R., et al. (2015). The khmer software package: enabling efficient nucleotide sequence analysis [version 1; referees: 2 approved, 1 approved with reservations]. F1000 Res. 4:900. doi: 10.12688/f1000research.6924.1
16. Dao, M., Everard, A., Aron-Wisnewsky, J., Sokolovska, N., Prifti, E., Verger, E., et al. (2016). Akkermansia muciniphila and improved metabolic health during a dietary intervention in obesity: relationship with gut microbiome richness and ecology. Gut 65, 426-436. doi: 10.1136/gutjnl-2014-308778
17. Di Rienzi, S. C., Sharon, I., Wrighton, K. C., Koren, O., Hug, L. A., Thomas, B. C., et al. (2013). The human gut and groundwater harbor non-photosynthetic bacteria belonging to a new candidate phylum sibling to Cyanobacteria. eLife 2:e01102. doi: 10.7554/eLife.01102
18. Eddy, S. R. (2011). Accelerated Profile HMM Searches. PLoS Comput. Biol. 7:e1002195. doi: 10.1371/journal.pcbi.1002195
19. Edgar, R. C. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460-2461. doi: 10.1093/bioinformatics/btq461
20. Eren, A. M., Esen, Ö. C., Quince, C., Vineis, J. H., Morrison, H. G., Sogin, M. L., et al. (2015). Anvi'o: an advanced analysis and visualization platform for 'omics data. PeerJ 3:e1319. doi: 10.7717/peerj.1319
21. Fierer, N., Hamady, M., Lauber, C., and Knight, R. (2008). The influence of sex, handedness, and washing on the diversity of hand surface bacteria. Proc. Natl. Acad. Sci. U.S.A. 105, 17994-17999. doi: 10.1073/pnas.0807920105
22. Fodor, A. A., DeSantis, T. Z., Wylie, K. M., Badger, J. H., Ye, Y., Hepburn, T., et al. (2012). The "most wanted" taxa from the human microbiome for whole genome sequencing. PLoS ONE 7:e41294. doi: 10.1371/journal.pone.0041294
23. Frey, B. J., and Dueck, D. (2007). Clustering by passing messages between data points. Science 315, 972-976. doi: 10.1126/science.1136800
24. Geirnaert, A., Steyaert, A., Eeckhaut, V., Debruyne, B., Arends, J., Van Immerseel, F., et al. (2014). Butyricicoccus pullicaecorum, a butyrate producer with probiotic potential, is intrinsically tolerant to stomach and small intestine conditions. Anaerobe 30, 70-74. doi: 10.1016/j.anaerobe.2014.08.010
25. Gevers, D., Knight, R., Petrosino, J. F., Huang, K., McGuire, A. L., Birren, B. W., et al. (2012). The Human Microbiome Project: a community resource for the healthy human microbiome. PLoS Biol. 10:e1001377. doi: 10.1371/journal.pbio.1001377
26. Handelsman, J. (2004). Metagenomics: application of genomics to uncultured microorganisms. Microbiol. Mol. Biol. Rev. 68, 669-685. doi: 10.1128/MMBR.68.4.669-685.2004
27. Handelsman, J., Rondon, M. R., Brady, S. F., Clardy, J., and Goodman, R. M. (1998). Molecular biological access to the chemistry of unknown soil microbes: a new frontier for natural products. Chem. Biol. 5, R245-R249. doi: 10.1016/S1074-5521(98)90108-9
28. Huerta-Cepas, J., Szklarczyk, D., Forslund, K., Cook, H., Heller, D., Walter, M. C., et al. (2015). eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences. Nucleic Acids Res. 44, D286-D293. doi: 10.1093/nar/gkv1248
29. Hyatt, D., LoCascio, P. F., Hauser, L. J., and Uberbacher, E. C. (2012). Gene and translation initiation site prediction in metagenomic sequences. Bioinformatics 28, 2223-2230. doi: 10.1093/bioinformatics/bts429
30. Immerseel, F. V., Ducatelle, R., Boon, N., Wiele, T. V. D., Verbeke, K., Rutgeerts, P., et al. (2010). Butyric acid-producing anaerobic bacteria as a novel probiotic treatment approach for inflammatory bowel disease. J. Med. Microbiol. 59(Pt 2), 141-143. doi: 10.1099/jmm.0.017541-0
31. Jeraldo, P., Hernández, A., White, B., O'Brien, D., Ahlquist, D., Boardman, L., et al. (2015). Draft genome sequences of 24 microbial strains assembled from direct sequencing from 4 stool samples. Genome Announc. 3:e5265. doi: 10.1128/genomeA.00526-15
32. Kuleshov, V., Jiang, C., Zhou, W., Jahanbani, F., Batzoglou, S., and Snyder, M. (2016). Synthetic long-read sequencing reveals intraspecies diversity in the human microbiome. Nat. Biotechnol. 34, 64-69. doi: 10.1038/nbt.3416
33. Lagesen, K., Hallin, P., Rødland, E. A., Staerfeldt, H.-H., Rognes, T., and Ussery, D. W. (2007). RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res. 35, 3100-3108. doi: 10.1093/nar/gkm160
34. Li, H., and Durbin, R. (2009). Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760. doi: 10.1093/bioinformatics/btp324
35. Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., et al. (2009). The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078-2079. doi: 10.1093/bioinformatics/btp352
36. Lok, C. (2015). Mining the microbial dark matter. Nature 522, 270-273. doi: 10.1038/522270a
37. Marakeby, H., Badr, E., Torkey, H., Song, Y., Leman, S., Monteil, C. L., et al. (2014). A system to automatically classify and name any individual genome-sequenced organism independently of current biological classification and nomenclature. PLoS ONE 9:e8912. doi: 10.1371/journal.pone.0089142
38. Martínez, I., Lattimer, J., Hubach, K., Case, J., Yang, J., Weber, C., et al. (2013). Gut microbiome composition is linked to whole grain-induced immunological improvements. ISME J. 7, 268-280. doi: 10.1038/ismej.2012.104
39. Mattick, J. (2002). Type IV pili and twitching motility. Annu. Rev. Microbiol. 56, 289-314. doi: 10.1146/annurev.micro.56.012302.160938
40. Meyer, F., Overbeek, R., and Rodriguez, A. (2009). FIGfams: yet another set of protein families. Nucleic Acids Res. 37, 6643-6654. doi: 10.1093/nar/gkp698
41. Morris, G. N., Winter, J., Cato, E. P., Ritchie, A. E., and Bokkenheuser, V. D. (1986). Eubacterium desmolans sp. nov., a steroid desmolase-producing species from cat fecal flora. Int. J. Syst. Bacteriol. 36, 183-186. doi: 10.1099/00207713-36-2-183
42. Nielsen, H. B., Almeida, M., Juncker, A. S., Rasmussen, S., Li, J., Sunagawa, S., et al. (2014). Identification and assembly of genomes and genetic elements in complex metagenomic samples without using reference genomes. Nat. Biotechnol. 32, 822-828. doi: 10.1038/nbt.2939
43. Parks, D. H., Imelfort, M., Skennerton, C. T., Hugenholtz, P., and Tyson, G. W. (2015). CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 25, 1043-1055. doi: 10.1101/gr.186072.114
44. Petkau, A., Stuart-Edwards, M., Stothard, P., and Van Domselaar, G. (2010). Interactive microbial genome visualization with GView. Bioinformatics 26, 3125-3126. doi: 10.1093/bioinformatics/btq588
45. Pignatelli M. (2014). Blast2lca. Available at: https://github.com/emepyc/Blast2lca
46. Price, M. N., Dehal, P. S., and Arkin, A. P. (2010). FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS ONE 5:e9490. doi: 10.1371/journal.pone.0009490
47. Qin, J., Li, R., Raes, J., Arumugam, M., Burgdorf, K. S., Manichanh, C., et al. (2010). A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464, 59-65. doi: 10.1038/nature08821
48. Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., et al. (2013). The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590-D596. doi: 10.1093/nar/gks1219
49. Quinlan, A. R. (2014). BEDTools: The Swiss-Army tool for genome feature analysis. Curr. Protoc. Bioinformatics 47, 11.12.11-11.12.34. doi: 10.1002/0471250953.bi1112s47
50. Reddy, T. B. K., Thomas, A. D., Stamatis, D., Bertsch, J., Isbandi, M., Jansson, J., et al. (2015). The Genomes OnLine Database (GOLD) v.5: a metadata management system based on a four level (meta)genome project classification. Nucleic Acids Res. 43, D1099-D1106. doi: 10.1093/nar/gku950
51. Richter, M., and Rosselló-Móra, R. (2009). Shifting the genomic gold standard for the prokaryotic species definition. Proc. Natl. Acad. Sci. U.S.A. 106, 19126-19131. doi: 10.1073/pnas.0906412106
52. Rosselló-Móra, R., and Amann, R. (2015). Past and future species definitions for Bacteria and Archaea. Syst. Appl. Microbiol. 38, 209-216. doi: 10.1016/j.syapm.2015.02.001
53. Ruby, J. G., Bellare, P., and Derisi, J. L. (2013). PRICE: software for the targeted assembly of components of (Meta) genomic sequence data. G 3, 865-880. doi: 10.1534/g3.113.005967
54. Schwiertz, A., Blay, G. L., and Blaut, M. (2000). Quantification of different Eubacterium spp. in human fecal samples with species-specific 16S rRNA-targeted oligonucleotide probes. Appl. Environ. Microbiol. 66, 375-382. doi: 10.1128/AEM.66.1.375-382.2000
55. Sharon, I., and Banfield, J. F. (2013). Genomes from metagenomics. Science 342, 1057-1058. doi: 10.1126/science.1247023
56. Sharon, I., Kertesz, M., Hug, L. A., Pushkarev, D., Blauwkamp, T. A., Castelle, C. J., et al. (2015). Accurate, multi-kb reads resolve complex populations and detect rare microorganisms. Genome Res. 25:gr.183012.183114. doi: 10.1101/gr.183012.114
57. Simpson, J. T., and Durbin, R. (2012). Efficient de novo assembly of large genomes using compressed data structures. Genome Res. 22, 549-556. doi: 10.1101/gr.126953.111
58. Snyder, E. E., Kampanya, N., Lu, J., Nordberg, E. K., Karur, H. R., Shukla, M., et al. (2007). PATRIC: the VBI PathoSystems Resource Integration Center. Nucleic Acids Res. 35, D401-D406. doi: 10.1093/nar/gkl858
59. Soo, R. M., Skennerton, C. T., Sekiguchi, Y., Imelfort, M., Paech, S. J., Dennis, P. G., et al. (2014). An expanded genomic representation of the phylum cyanobacteria. Genome Biol. Evol. 6, 1031-1045. doi: 10.1093/gbe/evu073
60. Stewart, E. (2012). Growing unculturable bacteria. J. Bacteriol. 194, 4151-4160. doi: 10.1128/JB.00345-12
61. Teeling, H., Meyerdierks, A., Bauer, M., Amann, R., and Glöckner, F. O. (2004). Application of tetranucleotide frequencies for the assignment of genomic fragments. Environ. Microbiol. 6, 938-947. doi: 10.1111/j.1462-2920.2004.00624.x
62. Tennessen, K., Andersen, E., Clingenpeel, S., Rinke, C., Lundberg, D. S., Han, J., et al. (2015). ProDeGe: a computational protocol for fully automated decontamination of genomes. ISME J. 10, 269-272. doi: 10.1038/ismej.2015.100
63. Torsvik, V., Goksøyr, J., and Daae, F. (1990). High diversity in DNA of soil bacteria. Appl. Environ. Microbiol. 56, 782-787
64. Vinolo, M., Rodrigues, H., Nachbar, R., and Curi, R. (2011). Regulation of inflammation by short chain fatty acids. Nutrients 3, 858-876. doi: 10.3390/nu3100858
65. Wood, D. E., and Salzberg, S. L. (2014). Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol. 15:R46. doi: 10.1186/gb-2014-15-3-r46
66. Zackular, J., Baxter, N., Iverson, K., Sadler, W., Petrosino, J., Chen, G., et al. (2013). The gut microbiome modulates colon tumorigenesis. MBio 4:e692. doi: 10.1128/mBio.00692-13
67. Zerbino, D. R., and Birney, E. (2008). Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18, 821-829. doi: 10.1101/gr.074492.107